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Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet in Drosophila


Hoedjes, Katja M; van den Heuvel, Joost; Kapun, Martin; Keller, Laurent; Flatt, Thomas; Zwaan, Bas J (2019). Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet in Drosophila. Evolution Letters, 3(6):598-609.

Abstract

Reproduction and diet are two major factors controlling the physiology of aging and life history, but how they interact to affect the evolution of longevity is unknown. Moreover, although studies of large-effect mutants suggest an important role of nutrient sensing pathways in regulating aging, the genetic basis of evolutionary changes in lifespan remains poorly understood. To address these questions, we analyzed the genomes of experimentally evolved Drosophila melanogaster populations subjected to a factorial combination of two selection regimes: reproductive age (early versus postponed), and diet during the larval stage ("low," "control," "high"), resulting in six treatment combinations with four replicate populations each. Selection on reproductive age consistently affected lifespan, with flies from the postponed reproduction regime having evolved a longer lifespan. In contrast, larval diet affected lifespan only in early-reproducing populations: flies adapted to the "low" diet lived longer than those adapted to control diet. Here, we find genomic evidence for strong independent evolutionary responses to either selection regime, as well as loci that diverged in response to both regimes, thus representing genomic interactions between the two. Overall, we find that the genomic basis of longevity is largely independent of dietary adaptation. Differentiated loci were not enriched for "canonical" longevity genes, suggesting that naturally occurring genic targets of selection for longevity differ qualitatively from variants found in mutant screens. Comparing our candidate loci to those from other "evolve and resequence" studies of longevity demonstrated significant overlap among independent experiments. This suggests that the evolution of longevity, despite its presumed complex and polygenic nature, might be to some extent convergent and predictable.

Abstract

Reproduction and diet are two major factors controlling the physiology of aging and life history, but how they interact to affect the evolution of longevity is unknown. Moreover, although studies of large-effect mutants suggest an important role of nutrient sensing pathways in regulating aging, the genetic basis of evolutionary changes in lifespan remains poorly understood. To address these questions, we analyzed the genomes of experimentally evolved Drosophila melanogaster populations subjected to a factorial combination of two selection regimes: reproductive age (early versus postponed), and diet during the larval stage ("low," "control," "high"), resulting in six treatment combinations with four replicate populations each. Selection on reproductive age consistently affected lifespan, with flies from the postponed reproduction regime having evolved a longer lifespan. In contrast, larval diet affected lifespan only in early-reproducing populations: flies adapted to the "low" diet lived longer than those adapted to control diet. Here, we find genomic evidence for strong independent evolutionary responses to either selection regime, as well as loci that diverged in response to both regimes, thus representing genomic interactions between the two. Overall, we find that the genomic basis of longevity is largely independent of dietary adaptation. Differentiated loci were not enriched for "canonical" longevity genes, suggesting that naturally occurring genic targets of selection for longevity differ qualitatively from variants found in mutant screens. Comparing our candidate loci to those from other "evolve and resequence" studies of longevity demonstrated significant overlap among independent experiments. This suggests that the evolution of longevity, despite its presumed complex and polygenic nature, might be to some extent convergent and predictable.

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Additional indexing

Item Type:Journal Article, refereed, further contribution
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Language:English
Date:1 December 2019
Deposited On:14 Feb 2020 14:14
Last Modified:16 Feb 2020 07:08
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:2056-3744
OA Status:Gold
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1002/evl3.143
PubMed ID:31867121
Project Information:
  • : FunderSNSF
  • : Grant ID310030B_176406
  • : Project TitleGenetic basis of alternative social organizations in fire ants
  • : FunderSNSF
  • : Grant IDPP00P3_165836
  • : Project TitleThe Genomic Basis of Life History Adaptation
  • : FunderSNSF
  • : Grant ID310030E-164207
  • : Project TitlePhysiological basis of the fecundity/longevity trade-off in Drosophila
  • : FunderH2020
  • : Grant ID741491
  • : Project TitleresiliANT - Resilience in ant societies
  • : FunderH2020
  • : Grant ID701949
  • : Project TitleEvolAge - Experimental Evolution of Aging: the genetic link between lifespan, nutrient sensing and fat metabolism

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